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Reproductive Ecology of Fucus Distichus (Phaeophyceae): an Intertidal Alga with Successful External Fertilization

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Reproductive Ecology of Fucus Distichus (Phaeophyceae): an Intertidal Alga with Successful External Fertilization MARINE ECOLOGY PROGRESS SERIES Vol. 143: 211-223,1996 Published November 14 Mar Ecol Prog Ser Reproductive ecology of Fucus distichus (Phaeophyceae):an intertidal alga with successful external fertilization Gareth A. Pearson*,Susan H. Brawley Department of Plant Biology and Pathology, University of Maine, Orono. Maine 04469. USA ABSTRACT: Patterns of natural gamete release and fertilization success are reported for the open-coast macrophyte Fucus distichus L. (formerly Fucus distichus ssp. distichus), which is restricted to tide pools in the upper intertidal zone. The release and settlement of eggs and zygotes of E distichus occurred during daytime low tide periods (DLT), largely on days when the low tide fell between 10:OO and 14:OO h EST; very few gametes were released when high tides fell during the same time interval. Gamete release during nighttime low tides was very low. During the DLT series, gametes were released in all pools and this was better correlated with the time of day than with time of low tide per se. The timing of fertilization showed considerable variation both within and between pools during a sin- gle DLT. No relationship between either pool temperature or osmolality and gamete release was evi- dent, and only small episodes of gamete release coincided with the times of full or new moons. The restriction of gamete release to periods of very low water motion, when tide pools are ~solatedby the low tide, prevents gamete dilution by water exchange and turbulent flows, and results in external fer- tilization success between 78 and loo'%)with low levels of polyspermy (l to 5%).Dispersal of zygotes among tide pools may be facilitated by the low winter temperatures during reproduction, which retard adhesive production and zygote attachment. Our results demonstrate that intertidal organisms, living in habitats characterized by periodic, turbulent flow regimes, Inay achieve high levels of fertilization success by releasing gametes under optimal hydrodynamic conditions for sperm-egg encounters. KEY WORDS: External fertilization success . Fertilization ecology . Fucoid algae . Fucus distichus . Gamete release . Polyspermy . Rocky intertidal zone INTRODUCTION umn; fertilization success under these conditions may be less than 1 D/o (Denny & Shibata 1989).Other studies Temporal variation in the supply of propagules (e.g. suggest that even those eggs that are fertilized may zygotes and larvae) to a comn~unitycan play a major still face damage from small-scale shear forces (Mead role in determining its structure (e.g.Gaines & Rough- & Denny 1994). Experimental field studies conducted garden 1985; reviewed by Underwood & Fairweather under less extreme hydrodynamic conditions have 1989). A key component of propagule supply for many confirmed that fertilization success declines with marine species is the success of external fertilization, a increasing water velocity (e.g.Pennington 1985, Levi- process that has long been a subject of scrutiny and tan et al. 1992; reviewed by Levitan & Petersen 1995 debate (e.g.Mortensen 1938, Thorson 1950; reviewed and Levitan 1995). However, to our knowledge, there by Levitan 1995). For example, recent modeling stud- have been no previous reports of natural patterns of ies predict that external fertilization is poorly suited to gamete release and external fertil~zationsuccess in an turbulent environments such as the intertidal zone intertidal organism on exposed shores. Fertilization because of rapid dilution of gametes in the water col- success during natural gamete release (spawning) in other habitats has been determined, i.e. in a few marine invertebrates (Babcock & Mundy 1992, Bab- ' Present address: U.C.T.R.A , Universidade do Algarve, Cam- pus de Gambelas, P-8000 Faro, Portugal. cock et al. 1992, Sewell & Levitan 1992, Babcock et al. E-mail. [email protected] 1994), fish (Petersen 1991, Petersen et al. 1992), and O Inter-Research 1996 Resale of full art~clenot permitted 212 Mar Ecol Prog Ser macroalgae (Brawley 1992, Serrao et al. 1996). High MATERIALS AND METHODS levels of fertilization success (ca 75 to 100%) were observed in these studies, except during a proportion Study site and preparation of pools. A total of 8 tide of the rougher days (Petersen 1991, Petersen et al. pools were studied between January and April 1995, 1992), or when ~ndividualsspawned in temporal or 4 In each of 2 moderately exposed sites at Chamber- spatial isolation (Babcock & Mundy 1992, Babcock et lain, Maine, USA (44"N,69' 30'E).Further studies of 2 al. 1992). Fertilization success was 95 to 100% in the of these pools were conducted during March 1996. Site estuarine, intertidal alga Fucus ceranoides, which A was situated on the eastern side of a rocky promon- mostly releases gametes near slack high tide, and tory (Long Cove Point), and Site B was located ca 50 m which has a semilunar periodicity of release (Brawley further east across the small, south facing bay (Fig 1). 1992). Continuously submerged populations of Fucus Both sites were characterized by granitic rock on sea- vesiculosus in the Baltic Sea also have high (>95%) ward-facing slopes of gentle to medium grade, with fertilization success, and are very responsive to turbu- the pools containing Fucus distichus (formerly F. dis- lent conditions, achieving high fertilization success by tichus ssp. distichus; Rice & Chapman 1985) being not releasing gametes when water velocities are high found just above the Fucus spiralis zone. Observations (Serrao et al. 1996). This suggests that spawning in of immersion time at high tide revealed that the pools marine organisms may be quite sensitive to water at Site A were flushed by waves for approximately 1 h velocity. If so, tide pools on exposed shores offer a tem- longer (ca 4 h) than those at Site B. During neap tides poral refuge from water motion that is particularly pre- coincident with calm seas, pools were sometimes dictable (Denny 1988). observed to be isolated from tidal input for 2 to 3 d. In this paper we describe natural gamete release and Preparation of the sites was carried out between Sep- fertilization success in the fucoid alga Fucus distichus tember and October 1994, prior to the onset of recepta- L., which is a monoecious species found exclusively in cle formation by the adult plants. A tape measure was tide pools in the upper littoral zone of moderately to placed along the long axis of each pool, and at 5 or very exposed rocky shores. Transplant experiments 10 cm intervals (depending on the size of the pool) the with microscopic early stages have demonstrated that distance to either edge was measured perpendicular to this species is physiologically incompetent to survive this axis; water depth was also determined at this time. on emergent rock, except in the lowest regions of the intertidal zone (Chapman & Johnson 1990), which is not its natural distribution. Male and female gametan- gia (antheridia and oogonia) are released from concep- tacles within the reproductive tips (receptacles) of the alga; conceptacles are spherical, sub-epidermal cham- bers connected via a pore to the surface, and each receptacle contains numerous conceptacles (Evans et al. 1982). Reproduction is seasonal, and the onset of receptacle formation occurs in late autumn in response to short days (Bird & McLachlan 1976).Gamete release occurs during the winter and early spring. Given the variations in temperature and salinity in tide pools dur- ing the winter in New England, USA, and eastern Subtidal I Canada (Edelstein & McLachlan 1975, this study), it is of interest to determine whether gamete release fol- lows the lunar or semilunar penodiclty found in several other macroalgae (Williams 1905, Fletcher 1980, Braw- ley 1992; references in Brawley & Johnson 1992), or occurs in response to different endogenous or environ- ----Splash Zone mental factors. Further, the synchrony of gamete 1 release between Individuals of monoecious species may be lower than that in dioecious species (Brawley 1992) if they are capable of self-fertilization, as mono- ecious fucoids are (Pollock 1970, S. H. Brawley pers. obs.). Our results show that fertilization is successful in Fig. 1. Study area at Chamberlain, Maine, USA (Long Cove F. distichus due to avoidance of gamete release under Point), showing the positions of tide pools containing Fucus turbulent conditions at high tide. distichus at Sites A and B Pearson & Bra~vley:Keproduct Ive ecology of Fucus distichus 213 film canister carefully onto the lid to seal the sample before lifting the assembly from the pool. The simplic- ity and rapidity of this system were advantages when working at low temperature, as samples were often collected from under thick ice cover. Sampling and field conditions. Daily sampling of eggs and zygotes was performed prior to immersion of the pools by a daytime or evening high tide (i.e. fol- lowing a daytime low tide). The disk assemblies were replaced with fresh ones on each occasion. Unlike many invertebrates, there is no larval stage in the life history of fucoid algae, and therefore settlement of eggs and zygotes into the shallow water of these iso- lated tide pools during the period of low tide directly reflects gamete release. Breaks in the daily sampling regime in 1995 occurred between January 31 and Feb- ruary 10 and between February 17 and 21. In addition, ice cover prevented sampling on several occasions when either (1) algae overlying settlement disks were embedded in the ice, preventing their removal to reach samples beneath, or (2) settlement disks were them- selves embedded in ice. On returning to the laboratory, Fig. 2. Settlement disk positioned in the substrate. The disk is held in place in a canister Lid that fits flush to a collar of Poxy both the settlement disk and the seawater in the canis- Putty, both flush with the substrate. The weighted bolt pro- ter were examined with a dissecting microscope, and trudes into the central hole to anchor the assembly.
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